POSTHARVEST DECAYS OF FLORIDA CITRUS FRUIT

G . ELDON BROWN

'INTRODUCTION

Fresh citrus fruit produced in a humid, high rainfall climate like Florida'sgenerally has potential for higher decay levels than fruit produced in more aridclimates. All of the fungi known to cause citrus decay can be found in Florida.Decay levels of 40-50% or more can occur within 2-3 weeks of harvest in extremeinstances without proper control measures. All costs of production, harvesting,packing and transportation are lost when decay occurs at the marketplace.

The intent in this discussion is to describe the various decays of Floridafresh citrus and the approaches to effective prevention and control. Consumerconfidence in our citrus fruit can be maintained only if it has consistently good

keeping quality.

DECAYS OF FLORmA CITRUS

The major postharvest diseases are listed in Table 1. The causal fungi eitherhave long quiescent periods of several months after invading the fruit beforelesions begin to develop or they begin to cause decay within days after infection.The lesions develop either at the stem-end from quiescent hyphae in necrotic tissueon the button (calyx and disk) surface, or anywhere on the intact or injured rindsurface from quiescent or germinating spores.

Stem-end Rot (Diplodia natalensis) - This is a major decay in the early seasonon degreened fruit. Spores of this-fungus are produced during the summer growingseason in pycnidia on deadwood in the tree canopy. They are carried in waterduring irrigation or rainfall to the button of the fruit where they germinate andbecome e~tablished in dead tissue of the button surface. After harvest, the fungusgrows through natural openings formed at abscission. Degreening enhances Diplodiastem-end rot because ethylene stimulates abscission. The temperature of 85F usedfor degreening is also optimum for the growth of this rapidly growing fungus, andthe high humidity required in the de greening room to prevent fruit desiccationfavors fungal growth.

The fungus penetrates the rind and core of the fruit at the stem-end. Thehyphae progress rapidly down the spongy core, usually reaching the stylar-end muchsooner by this route, than through the rind. The decay proceeds unevenly throughthe rind, thereby producing finger-like projections of brown or black tissue.Typically, the decay appears at both the stem and stylar ends of the fruit beforeinvolving the whole fruit. Initially, the decay is firm; but later it becomes wetand mushy. Surface mycelium appears only at advanced stages of infection in verymoist environments. The decay does not usually spread from infected to healthyfruit in packed containers.

Anthracnose (Collectotrichum gloeosporioides) - This is R major decay of .onlyde greened Robinson tangerines. Spores are produced in acervuli on deadwood in thetree canopy and carried in water to fruit surfaces during summer rains. Sporesgerminate and form appressoria which remain quiescent until fruit are treated withethylene during degreening. Ethylene stimulates the appressoria to germinate andform infection hyphae which penetrate the uninjured rind, particularly whendegreening exceeds 36 hours. The lesions may occur around the button or on anyportion of the fruit. They appear firm and silvery-grey and later become softerand brown to black in color. Anthracnose may also develop in the absence ofethylene, but only at injuries, bruises or otherwise weakened areas of the fruitsurface.

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Major postharvest diseases of Florida citrus fruit, causal fungiand type, site and spread of infection.

Table 1.

Disease Causal fungus

NoAnthracnose Colletotrichum Quiescent Intact orinjured rindgloeosporioides

Active Intact rindBrown rot Phytophthora citrophthoraPhytophthora parasitica

Injured rind NoGreen mold Penicillium digitatum Active

Injured rindGeotrichum candidum. ActiveSour rot

Natural openingsat the stem-end

Stem-end rot PhO8)psis ~ NoQuiescent

Alternaria citrl Natural openingsat the stem-end

NoQuiescentStem-end rot(Black rot)

Brown rot (Phytophthora citrophthora, !.::. parasitica) - Brown rot is alocalized disease, most frequently found on the East Coast, that may recur yearafter year in the same grove. It may be severe in seasons with unusually longdurations of rainfall and wetting caused by slow-moving tropical depressions orhurricanes. Such conditions are more likely to occur in the early fall than laterin the season and therefore, it is mostly the early maturing cultivars that areaffected. Significant losses are attributed to !.::. citrophthora which has thepotential to produce more inoculum than !.::. parasitica under comparable climaticconditions. Under wet conditions, zoospores are splashed from the soil onto lowhanging fruit. Spores can be produced on these fruit and then be splashed higherinto the canopy. Infected fruit surfaces are firm and leathery, light todark-brown and retain the same degree of firmness and elevation as the surroundinghealthy surfaces. Delicate white mycelium forms on the rind under humidconditions. Fruit infected with Phytophthora have a characteristic pungent rancidodor. The disease can spread from infected to healthy fruit in packed cartons.

Green ~ld (Penicilliua digitatum) - This is a major decay which develops onlyif there are injuries in the rind, but even minor injuries involving only a few oilglands are sufficient to allow infection. Spores of the fungus are airborne andare produced on the surfaces of infected fruit. Large numbers of these spores areproduce4 during the winter months by infections in the grove on fallen, split fruitand in the packinghouse on injured fruit. Initially, the decay appears as a soft,watery, slightly discolored spot. After a few days, sparce white mycelium developson the lesion surface followed by the production of olive-green spores. Thesporulating area is surrounded by a broad zone of white mycelium and an outer zoneof softened rind. Spores are easily dispersed if the fruit is handled or shaken orif it is exposed to air currents. Spores from infected fruit in packed cartons

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.

will affect the value of the healthy fruit by settling on them and causing 80ilage.The decay doe. Dot spread from infected to healthy fruit in packed carton..

The incidence of green aold i8 decrea.ed by the condition. used in thedegreening proce.8. High teaperatures and huaidities of the degreening room favorthe bealing of any 8uperficial injuries in the flavedo. The fungus grows slowly atthe bigh degreening rooa te.perature and i8 unable to penetrate many of theinjurie8 before they beal and fora a barrier to infection.

Sour rot (Geotrichua candidua) - 111is is a major decay of specialty fruits.

such as tangerines, tangelos and 'Temple' oranges, and of quite mature roundoranges and grapefruit. Infection. occur .o8tly through th08e injuries that extendinto the albedo. 111e fungu8 is present in the soil and is 8Ore prevalent on loverfruit of the tree canopy e8pecially in dirt and debris on .carred fruit surfaces orunder the button. The fungus ..y not produce an active lesion unle8s the peel hasa relatively high wter content am the fruit are held at high relative htDidities.

Initial 8yapt088 of sour rot are 8iailar to tho.e of green and blue mold. Thelesion fir8t appears water-80aked, light to dark yellow, and slightly raiaed. 111ecuticle i. more easily r-.oved froa the epidermi8 than froa le8ion8 formed byPenicilliua. At high relative humidities, the le8ion may be covered with a yeasty,.o.eti.e8 wrinkled layer of white or cre.. colored .yceliua. The fungu8 degradesthe fruit thoroughly, cauaing it to disintegrate into a 8limy and watery ..88.

Fruit flie8 are attracted to 80ur rot and will spread inoculua fro. infectedto healthy injured fruit 1n the packinghou8e. Hyphae in rotted fruit fragment intochains of spores which contaainate packinghou8e equi~nt and water in drenchersand soak tanka. Sour rot will 8pread fro. infected to healthy fruit in packedcarton. and throughout cartons in a stack during 8torage or export. Sour rot 1soften a..ociated with green .old and is 8timulated by ita presence.

Ste.-end rot (Phomopsis £!!!!) - This aajor decay is 8Ore prevalent during thecooler winter .onth8 or in fruit placed in cold 8torage for SU888r 8ale. The lifecycle of thi8 fungu8, which also cause8 .-lanose, is siailar to that de8cribed forDiplodia. PhO8OP8i8 develops 8Ore slowly than Diplodia, and it usually cauees 808e8hriveling of the decayed tia8ue at the stea-end of the fruit. A clear line ofd...rcation is formed at the junction between disea8ed and healthy rind. DecaycaU8es a tan or brown discoloration, and progre.ses equally rapidly through thecore and rind until the entire fruit is enco.passed. The decay does not spreadfro. infected to healthy fruit in packed cartons.

Ste.-end rot (Alternar1a citri) - This 8inor decay can develop either at the

stylar or stea-ends of the fruit, cau8ing black discoloration of the peel and core.Airborne spores in the grove produced on ground litter infect dead tissue of thebutton and tissues at the stylar-end through growth cracks. Quiescent infectionsat the stylar-end of navel oranges and 'Orlando' tangelos, in particular, willcause premature color break and fruit drop. Infections at the stea-end, si8ilar tothose caused by Diplodia and Phoaopsis, develop after harvest but only afterlengthy storage. Ste8-end rot is not normally found in fruit consumed within3-4 week., but does develop in 8-10 weeks in oranges or grapefruit stored forsu..er sale. In S08e fruit, the fungus develops internally and reaains undetecteduntil the fruit is peeled for eating. At that time, the core will be composed ofrotted, black tissue (black rot).

Blue 8)ld (Penicilliua italicua) - 111is is a ainor decay with a life cyclelike 1. digitatua. Blue mold develops less rapidly than green mold at &abienttemperatures, but will still develop at low temperature8. It i8, therefore, soreoften encountered than green .old in fruit held in cold storage.

Initial SyaptO8B are very 8i.llar to those of sour rot. 111e disea8ed tissue

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is soft, watery, slightly discolored, and easily punctured. The lesions do notenlarge as rapidly as those of green mold. A white, powdery growth of myceliumdevelops on the lesion surface and is soon followed by the development of a bluespore mass, leaving only a narrow white fringe of .ycelium around the lesion. Apronounced halo of water-soaked, faded tissue is present between the fringe of.ycelium and sound tissue. Blue .old, unlike green mold, will also spread inpacked cartons causing pockets of diseased fruit to develop. In addition, bluemold also creates a problea in packed cartons through soilage, as with green mold.

Control of Po8tharvest Diseases

Cultural practices - Some cultural practices have been shown to reduce certainpostharvest diseases by affecting inoculum production. Incidences of Diplodia andPhomopsis stem-end rot are less in fruit harvested from trees with small amounts ofdead wood in the canopy. Trees with less dead wood can be produced by usingeffective cultural practices and by pruning dead wood from the tree canopy. Brownrot is reduced by cultural practices which minimize long periods of wetness in thefield. These are proper irrigation management, mowing to prevent ground vegetationgrowing too tall, pruning to remove low hanging branches, and soil drainage.

Harvesting practices- Care in harvesting is as important as fungicidetreataent for reducing decay development. By minimizing scratches, punctures andplugging with careful harvesting and handling, the 2 major wound decays, green moldand sour rot, can be reduced significantly. Contamination by the sour rot funguscan be minimized by preventing the fruit from contacting the soil during harvest.Harvesting by pulling rather than clipping can reduce the incidence of Diplodiastem end rot (SER) by removing at least some of the buttons that harbor the

pathogen.

Diplodia SER and anthracnose can be reduced if the degreening time isdecreased by spot-picking for natural color or by delaying harvest until more colordevelops. Following known infection periods of brown rot, harvesting should bedelayed for 4 to 6 days until infected fruit drop to the ground to minimize the

risk of infected fruit reaching the packinghouse.

Packinghouse practices - Effective and careful packinghouse handling is needed

to prevent fruit desiccation and injuries that encourage decay development. Properconditions of humidity, ethylene and temperature should be maintained duringdegreening and storage. Diplodia SER and anthracnose are significantly enhanced byethylene concentrations exceeding those required for optimal degreening. Humiditylevels of at least 90% are required durinK degreening to heal minor injuries and

enhance resistance to green mold.Airborne populations of Penicilliua can be minimized by exhausting spores from

the dump area and controlling air movement from the dump to the packing area.Sanitary practices should be applied to prevent the accumulation of spores onequipment surfaces, in treating solutions, and in the atmosphere of the packing andstorage facilities. Disinfectants such as chlorine, quaternary ammonium chloride,formaldehyde and alcohol are useful for preventing inoculum build-up of green mold

and sour rot.Airborne populations of Penicillium should be routinely checked for resistance

to postharvest fungicides. Fungicide-treated fruit infected with Penicilliumshould never be repacked in the packinghouse for the fear of releasing resistantspores into the atmosphere. Alternate applications or mixtures of fungicides ofunrelated chemistry should be used to suppress sporulation and to delay the

possible buildup of resistance.Immediate cooling of packed fruit effectively delays development of decay,

particularly Diplodia SER and sour rot.

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Table 2. Relative effectiveness of the approved postharvest fungicidesagainst citrus fruit decay.

Green Blue Sour Brown.Fungicide Diplodia Phomopsi8 Alternaria mold mold rot Anthracnose rot

...8 --- - .-- --- - --Thiabendazo le +++ +++ 0 +++ +++ 0 + 0Benomy 1 +++ +++ 0 +++ +-H- 0 ++ 0SOppY + + 0 ++ ++ + 0 0Diphenyl + + 0 - ++ ++ 0 0 0Imazalil ++ ++ + +++ +++ 0 0 0

Stem-end rot

- " .~ I

Z Control: 0 - none; + - 80me; ++ - moderate; +++ - good - c::;.:"~!;'I(;y Sodium orthophenylphenate ~~f~"L-.i':

Chemical control - Effective control of the major decays except sour rot can

be obtained with fungicides. An objective rating of the efficacy of the fungicidesapproved for citrus is presented in Table 2. Thiabendazole and benomyl arechemically similar as are SOPP and diphenyl. Penicillium digitatum and ~ .italicum

can become resistant to fungicides, but development occurs more slowly to imazalilthan to the other fungicides. Specific whole fruit residue tolerances areestablished for each fungicide and these may vary somewhat among countries. Forexample, Japan has established tolerances only for thiabendazole, SOPP anddiphenyl.

Field use of fungicides for the control of postharvest diseases is restrictedto applications of copper or benomyl. Copper can be applied as early as August orSeptember to early- or mid-season cultivars for controlling brown rot. A s'econdtreatu.nt may be needed if the year is unusually wet. Benomyl can be appliedwithin 3 weeks of harvest, and it is applied particularly to provide protectionagainst Diplodia SER and green mold when the postharvest fungicide treatment isdelayed, as it may be if the fruit has to be degreened. Use of the benomyl spraymay encourage buildup of resistant strains of green mold in the field which thenare not effectively controlled with applications of benomyl or thiabendazole in the

packinghouse.Control of decay in degreened fruit can also be achieved by applying drenches

of benomyl or thiabendazole to pallets of fruit before degreening. Treatments havebeen applied to pallets on the truck or after unloading. Fungicide suspensionsshould be chlorinated (50-100 ppm free, active chlorine, pH 6.5-7.5) to eradicate~ ~~id~, Phytophthora ,!EE.. and resistant spores of Penicillium that mayaccumulate in the drencher. Once the drench suspension becomes dirty, anenvironmentally safe procedure is required for disposal.

Sodium orthophenylphenate is commonly applied in a drench or foam during thewashing process for decay control and for disinfecting fruit to comply with thecanker regulations. Not only does this treatment provide some control of decay ininfected fruit, it also sanitizes the brushes and reduces contamination of healthyfruit by Penicillium or Geotrichum. Recovery drench applications of SOPP for 2minutes provide better decay control than foam applications for 30-45 seconds. Thefungicide may be phytotoxic if proper pH and treatment time and conditions are notmaintained, particularly on tender, early-season degreened fruit.

Benomyl, thiabendazole or imazalil are commonly applied in aqueous non-recovery sprays or mists to washed fruit rotating on brushes saturated with thefungicide. Problems with contamination or dilution do not occur with this systemlike they do in recovery drenches. Excess water should be removed from the washedfruit to prevent dilution of the fungicide. Removal of some of the fungicideresidues by brushes in polisher-driers may occur and possibly reduce efficacy of

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imazalil against sporulation of Penicillium. With the increased use of waterwaxes, many packinghouses apply benomyl, thiabendazole or imazalil in the wax in asimilar nonrecovery application. Since some loss in efficacy occurs, concentra-tions of the fungicides are doubled in wax applications. Even then, control withiaazalil of Dip10dia SER or green mold developing in post treatment injuries is notas effective as with aqueous applications. Benomy1 is unstable in highly alkalinewater waxes (pH 9-10), and suspensions should be used immediately. Equipmentbreakdowns that interrupt the fungicide applications are quickly discerned becauseof the lack of wax coverage.

Diphenyl is a volatile fungistat that prevents decay only while an effectiveconcentration is present in the atmosphere surrounding the fruit. The major use ofthe sateria1 is to prevent sporulation of Penicillium. The fungistat isimpregnated into pads that are inserted in the carton at packing. These pads mustbe stored in air-tight containers before use to prevent loss of diphenyl. Earlyharvested fruit and fruit stored at higher temperatures tend to absorb morediphenyl. Oranges and mandarins absorb at least twice as auch dipheny1 per unit offruit surface as lemons or grapefruit. The odor iaparted in diphenyl isobjectionable to some consumers. However, it is detectable for only 2 or 3 daysafter fruit are reaoved froa the atmosphere. Decays will resume development withina week after the fruit are removed from the diphenyl vapors.

SUMMARY

Good cultural, harvesting, handling and fungicide practices culminate ineffective decay control. Lack of attention to anyone of these factors will reducecontrol efficiency. With the recent development of some quite effectivefungicides, the fresh fruit industry has tended to place less emphasis on theseother factors, particularly that of good harvesting practices. The importance ofcareful harvesting can not be overemphasized because, in spite of effectivefungicides, keeping quality of some cultivars, particularly 'Dancy' tangerine, hasbeen deteriorating over the last few years. If present harvesting practicespersist, the 'Dancy' may eventually disappear from the market.

REFERENCES

Brown, G. E. 1980. Fruit handling and decay control techniques affecting quality.. pp. 193-224. In: Citrus Nutrition and Quality. S. Nagy and J. A. Attaway

(Editors). American Chemical Society Symposium Series 143, Washington, DC.Dezman, D. J., Nagey, S. & Brown, G. E. 1986. Postharvest fungal decay control

cheaica1s: Treatments and residues in citrus fruits. Residue Reviews 97:

37-92.Eckert, J. W. & BrCMl, G. E. 1986. Postharvest citrus diseases and their control.

pp. 315-360. In: Fresh Citrus Fruits. W. F. Wardowski, S. Nagy and W.Grierson (Editors). Avi Pub1. Co., Inc., Westport, Conn.

Eckert, J. W. & Wild, B. L. 1983. Problems of fungicide res~stance in penicilliumrot of citrus fruits. pp.525-556. In: Pest Resistance to Pesticides. G. P.Georghiou and T. Saito (Editors). Plenum Press, New York, NY.

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